Cite this paper:
Kai WANG, Xin WANG, Qiang ZOU, Han JIANG, Rongrong ZHANG, Yanan TIAN, Lele ZHANG, Qiang LIN. Genome-wide evolution of MAPKs family and their expression in response to bacterial infection in seahorse Hippocampus erectus[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2309-2321

Genome-wide evolution of MAPKs family and their expression in response to bacterial infection in seahorse Hippocampus erectus
Kai WANG1, Xin WANG2,3, Qiang ZOU4, Han JIANG2,5, Rongrong ZHANG2,5, Yanan TIAN1, Lele ZHANG1, Qiang LIN2,3,5
1 School of Agriculture, Ludong University, Yantai 264025, China;
2 CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China;
3 Southern Marine Science and Engineering Guangdong Laboratory(Guangzhou), Guangzhou 511458, China;
4 Yantai Branch of Shandong Technology Transfer Center, Chinese Academy of Sciences, Yantai 264003, China;
5 University of Chinese Academy of Sciences, Beijing 100049, China
Abstract:
Seahorses have evolved many unique biological traits, including a male brood pouch, the absence of caudal and pelvic fins, and the lack of spleen and gut-associated lymphatic tissue. The mitogenactivated protein kinases (MAPKs) are known to be involved in various important biological processes including growth, differentiation, immunity, and stress responses. Therefore, we hypothesized that the adaptive evolution and expression of the MAPK gene family in seahorse may differ from those of other teleost species. We identified positive selection sites in the erk2, erk5, jnk1, and p38α MAPK genes of the lined seahorse Hippocampus erectus and tiger-tailed seahorse Hippocampus comes. A novel expression profile of MAPK cascade genes was found in seahorse larvae during the first day after birth based on the RNA-seq data of H. erectus, which reflected vital signs of immune response to its parental immune system. The expression patterns of the four positively selected MAPK genes were analyzed following the bacterial challenge of Vibrio fortis, revealing their upregulation pattern in brood pouch and other immune tissues. This study enriched our knowledge of the evolution of the H. erectus MAPK subfamilies, and could help better understanding the functional role of MAPKs in teleosts.
Key words:    mitogen-activated protein kinases (MAPKs)|Hippocampus erectus|genomic structure|positive selection|immune regulation   
Received: 2020-08-25   Revised: 2020-11-09
Tools
PDF (2246 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by Kai WANG
Articles by Xin WANG
Articles by Qiang ZOU
Articles by Han JIANG
Articles by Rongrong ZHANG
Articles by Yanan TIAN
Articles by Lele ZHANG
Articles by Qiang LIN
References:
Abascal F, Zardoya R, Posada D. 2005. ProtTest:selection of best-fit models of protein evolution. Bioinformatics, 21(9):2104-2105, https://doi.org/10.1093/bioinformatics/bti263.
Antonopoulou E, Kentepozidou E, Feidantsis K, Roufidou C, Despoti S, Chatzifotis S. 2013. Starvation and re-feeding affect Hsp expression, MAPK activation and antioxidant enzymes activity of European sea bass (Dicentrarchus labrax). Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 165(1):79-88, https://doi.org/10.1016/j.cbpa.2013.02.019.
Arthur J S C, Ley S C. 2013. Mitogen-activated protein kinases in innate immunity. Nature reviews Immunology, 13(9):679-692, https://doi.org/10.1038/nri3495.
Cargnello M, Roux P P. 2011. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiology and Molecular Biology Reviews, 75(1):50-83, https://doi.org/10.1128/MMBR.00031-10.
Codina M, García de la serrana D, Sánchez-Gurmaches J, Montserrat N, Chistyakova O, Navarro I, Gutiérrez J. 2008. Metabolic and mitogenic effects of IGF-Ⅱ in rainbow trout (Oncorhynchus mykiss) myocytes in culture and the role of IGF-Ⅱ in the PI3K/Akt and MAPK signalling pathways. General and Comparative Endocrinology,157(2):116-124, https://doi.org/10.1016/j.ygcen.2008.04.009.
Cook J G, Bardwell L, Thorner J. 1997. Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signalling pathway. Nature, 390(6655):85-88, https://doi.org/10.1038/36355.
Coulombe P, Meloche S. 2007. Atypical mitogen-activated protein kinases:structure, regulation and functions. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1773(8):1376-1387, https://doi.org/10.1016/j.bbamcr.2006.11.001.
Ding X, Liang Y S, Peng W, Li R Z, Lin H R, Zhang Y, Lu D Q. 2018. Intracellular TLR22 acts as an inflammation equalizer via suppression of NF-κB and selective activation of MAPK pathway in fish. Fish & Shellfish Immunology, 72:646-657, https://doi.org/10.1016/j.fsi.2017.11.042.
Feidantsis K, Pörtner H O, Markou T, Lazou A, Michaelidis B. 2012. Involvement of p38 MAPK in the induction of Hsp70 during acute thermal stress in red blood cells of the gilthead sea bream, Sparus aurata. Journal of Experimental Zoology Part A-Ecological Genetics and Physiology, 317(5):303-310, https://doi.org/10.1002/jez.1725.
Foster S J, Vincent A C J. 2004. Life history and ecology of seahorses:implications for conservation and management. Journal of Fish Biology, 65(1):1-61, https://doi.org/10.1111/j.0022-1112.2004.00429.x.
Fuentes E N, Björnsson B T, Valdés J A, Einarsdottir I E, Lorca B, Alvarez M, Molina A. 2011. IGF-I/PI3K/Akt and IGF-I/MAPK/ERK pathways in vivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder. American Journal of Physiology, Regulatory, Integrative and Comparative Physiology, 300(6):1532-1542, https://doi.org/10.1152/ajpregu.00535.2010.
Galtier N, Nabholz B, Glémin S, Hurst G D D. 2009. Mitochondrial DNA as a marker of molecular diversity:a reappraisal. Molecular Ecology, 18(22):4541-4550, https://doi.org/10.1111/j.1365-294X.2009.04380.x.
Guindon S, Dufayard J F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies:assessing the performance of PhyML 3.0. Systematic Biology, 59(3):307-321, https://doi.org/10.1093/sysbio/syq010.
Hamel L P, Nicole M C, Duplessis S, Ellis B E. 2012. Mitogenactivated protein kinase signaling in plant-interacting fungi:distinct messages from conserved messengers. Plant Cell, 24(4):1327-1351, https://doi.org/10.1105/tpc.112.096156.
He Y, Cai C, Sun S, Wang X, Li W, Li H. 2016. Effect of JNK inhibitor SP600125 on hair cell regeneration in zebrafish(Danio rerio) larvae. Oncotarget, 7:51640-51650, https://doi.org/10.18632/oncotarget.10540.
Iliev D B, Hansen T, Jørgensen S M, Krasnov A, Jørgensen J B. 2013. CpG- and LPS-activated MAPK signaling in in vitro cultured salmon (Salmo salar) mononuclear phagocytes. Fish & Shellfish Immunology, 35(4):1079-1085, https://doi.org/10.1016/j.fsi.2013.07.014.
Inoue J, Sato Y, Sinclair R, Tsukamoto K, Nishida M. 2015. Rapid genome reshaping by multiple-gene loss after whole-genome duplication in teleost fish suggested by mathematical modeling. Proceedings of the National Academy of Sciences of the United States of America, 112(48):14918-14923, https://doi.org/10.1073/pnas. 1507669112.
Jia Q J, Fan Z J, Yao C L. 2015. Identification and expression profiles of erk2 and erk5 in large yellow croaker(Larimichthys crocea) after temperature stress and immune challenge. Fish & Shellfish Immunology, 44(2):410-419, https://doi.org/10.1016/j.fsi.2015.03.006.
Jopling C, Suñè G, Morera C, Izpisua Belmote J C. 2012. p38α MAPK regulates myocardial regeneration in zebrafish. Cell Cycle, 11(6):1195-1201, https://doi.org/10.4161/cc.11.6.19637.
Katoh K, Standley D M. 2013. MAFFT multiple sequence alignment software version 7:improvements in performance and usability. Molecular Biology and Evolution, 30(4):772-780, https://doi.org/10.1093/molbev/mst010.
Kawaguchi, M, Hiroi, J, Miya, M, Nishida, M, Iuchi, I, Yasumasu, S, 2010. Intron-loss evolution of hatching enzyme genes in Teleostei. BMC Evolutionary Biology, 10:260, https://doi.org/10.1186/1471-2148-10-260.
Keller J M, Escara-Wilke J F, Keller E T. 2008. Heat stressinduced heat shock protein 70 expression is dependent on ERK activation in zebrafish (Danio rerio) cells. Comparative Biochemistry and Physiology Part A:Molecular & Integrative Physiology, 150(3):307-314, https://doi.org/10.1016/j.cbpa.2008.03.021.
Krens S F G, He S N, Lamers G E M, Meijer A H, Bakkers J, Schmidt T, Spaink H P, Snaar-Jagalska B E. 2008. Distinct functions for ERK1 and erk2 in cell migration processes during zebrafish gastrulation. Developmental Biology, 319(2):370-383, https://doi.org/10.1016/j.ydbio.2008.04.032.
Krens S F G, He S N, Spaink H P, Snaar-Jagalska B E. 2006. Characterization and expression patterns of the MAPK family in zebrafish. Gene Expression Patterns, 6(8):1019-1026, https://doi.org/10.1016/j.modgep.2006.04.008.
Kültz D, Avila K. 2001. Mitogen-activated protein kinases are in vivo transducers of osmosensory signals in fish gill cells. Comparative Biochemistry and Physiology Part B:Biochemistry and Molecular Biology, 129(4):821-829, https://doi.org/10.1016/s1096-4959(01)00395-5.
Kyriakis J M, Avruch J. 2012. Mammalian MAPK signal transduction pathways activated by stress and inflammation:a 10-year update. Physiological Reviews, 92(2):689-737, https://doi.org/10.1152/physrev.00028.2011.
La Rocca C, Carbone F, Longobardi S, Matarese G. 2014. The immunology of pregnancy:regulatory T cells control maternal immune tolerance toward the fetus. Immunology Letters, 162(1):41-48, https://doi.org/10.1016/j.imlet. 2014.06.013.
Leal R B, Ribeiro S J, Posser T, Cordova F M, Rigon A P, Filho E Z, Bainy A C D. 2006. Modulation of ERK1/2 and p38MAPK by lead in the cerebellum of Brazilian catfish Rhamdia quelen. Aquatic Toxicology, 77(1):98-104, https://doi.org/10.1016/j.aquatox.2005.11.002.
Li M, Liu J, Zhang C Y. 2011. Evolutionary history of the vertebrate mitogen activated protein kinases family. PLoS One, 6(10):e26999, https://doi.org/10.1371/journal.pone.0026999.
Li X Y, Ma J G, Li Y Y. 2016. Molecular cloning and expression determination of p38 MAPK from the liver and kidney of silver carp. Journal of Biochemical and Molecular Toxicology, 30(5):224-231, https://doi.org/10.1002/jbt. 21781.
Lin Q, Fan S H, Zhang Y H, Xu M, Zhang H X, Yang Y L, Lee A P, Woltering J M, Ravi V, Gunter H M, Luo W, Gao Z X, Lim Z W, Qin G, Schneider R F, Wang X, Xiong P W, Li G, Wang K, Min J M, Zhang C, Qiu Y, Bai J, He W M, Bian C, Zhang X H, Shan D, Qu H Y, Sun Y, Gao Q, Huang L M, Shi Q, Meyer A, Venkatesh B. 2016. The seahorse genome and the evolution of its specialized morphology. Nature, 540(7633):395-399, https://doi.org/10.1038/nature20595.
Lin Q, Qiu Y, Gu R B, Xu M, Li J, Bian C, Zhang H X, Qin G, Zhang Y H, Luo W, Chen J M, You X X, Fan M J, Sun M, Xu P, Venkatesh B, Xu J M, Fu H T, Shi Q. 2017. Draft genome of the lined seahorse, Hippocampus erectus. Giga Science, 6(6):1-6, https://doi.org/10.1093/gigascience/gix030.
Litman G W, Rast J P, Fugmann S D. 2010. The origins of vertebrate adaptive immunity. Nature Reviews Immunology, 10(8):543-553, https://doi.org/10.1038/nri2807.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25(4):402-408, https://doi.org/10.1006/meth.2001.1262.
Luo W, Wang X, Qu H Y, Qin G, Zhang H X, Lin Q. 2016. Genomic structure and expression pattern of MHC Ⅱα and Ⅱ β genes reveal an unusual immune trait in lined seahorse Hippocampus erectus. Fish & Shellfish Immunology, 58:521-529, https://doi.org/10.1016/j.fsi. 2016.09.057.
Marshall W S, Cozzi R R F, Spieker M. 2017. WNK1 and p38-MAPK distribution in ionocytes and accessory cells of euryhaline teleost fish implies ionoregulatory function. Biology Open, 6(7):956-966, https://doi.org/10.1242/bio.024232.
Marshall W S, Ossum C G, Hoffmann E K. 2005. Hypotonic shock mediation by p38 MAPK, JNK, PKC, FAK, OSR1 and SPAK in osmosensing chloride secreting cells of killifish opercular epithelium. Journal of Experimental Biology, 208(Pt 6):1063-1077, https://doi.org/10.1242/jeb.01491.
Matsunaga T, Rahman A. 1998. What brought the adaptive immune system to vertebrates?-The jaw hypothesis and the seahorse. Immunological Reviews, 166(1):177-186, https://doi.org/10.1111/j.1600-065x.1998.tb01262.x.
Olavarria V H, Valdivia S, Salas B, Villalba M, Sandoval R, Oliva H, Valdebenito S, Yañez A. 2015. ISA virus regulates the generation of reactive oxygen species and p47 phox expression in a p38 MAPK-dependent manner in Salmo salar. Molecular Immunology, 63(2):227-234, https://doi.org/10.1016/j.molimm.2014.07.016.
Plotnikov A, Zehorai E, Procaccia S, Seger R. 2011. The MAPK cascades:signaling components, nuclear roles and mechanisms of nuclear translocation. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1813(9):1619-1633, https://doi.org/10.1016/j.bbamcr.2010.12.012.
Qin G, Zhang Y H, Ho A L F C, Zhang Y, Lin Q. 2017. Seasonal distribution and reproductive strategy of seahorses. ICES Journal of Marine Science. 74(8):2170-2179, https://doi.org/10.1093/icesjms/fsx042.
Raman M, Chen W, Cobb M H. 2007. Differential regulation and properties of MAPKs. Oncogene, 26(22):3100-3112, https://doi.org/10.1038/sj.onc.1210392.
Roth O, Solbakken M H, Tørresen O K, Bayer T, Matschiner M, Baalsrud H T, Hoff S N K, Brieuc M S O, Haase D, Hanel R, Reusch T B H, Jentoft S. 2020. Evolution of male pregnancy associated with remodeling of canonical vertebrate immunity in seahorses and pipefishes. Proceedings of the National Academy of Sciences of the United States of America, 117(17):9431-9439, https://doi.org/10.1073/pnas.1916251117.
Sánchez-Gurmaches J, Cruz-Garcia L, Ibarz A, FernándezBorrás J, Blasco J, Gutiérrez J, Navarro I. 2013. Insulin, IGF-I, and muscle MAPK pathway responses after sustained exercise and their contribution to growth and lipid metabolism regulation in gilthead sea bream. Domestic Animal Endocrinology, 45(3):145-153, https://doi.org/10.1016/j.domaniend.2013.08.001.
Sémon M, Wolfe K H. 2007. Rearrangement rate following the whole-genome duplication in teleosts. Molecular Biology and Evolution, 24(3):860-867, https://doi.org/10.1093/molbev/msm003.
Sopontammarak S, Aliharoob A, Ocampo C, Arcilla R A, Gupta M P, Gupta M. 2005. Mitogen-activated protein kinases (p38 and c-Jun NH2-terminal kinase) are differentially regulated during cardiac volume and pressure overload hypertrophy. Cell Biochemistry and Biophysics, 43(1):61-76, https://doi.org/10.1385/CBB:43:1:061.
Sun Y, Zhang L L, Zhang M W, Li R J, Li Y P, Hu X L, Wang S, Bao Z M. 2016. Characterization of three mitogenactivated protein kinases (MAPK) genes reveals involvement of ERK and JNK, not p38 in defense against bacterial infection in Yesso scallop Patinopecten yessoensis. Fish & Shellfish Immunology, 54:507-515, https://doi.org/10.1016/j.fsi.2016.04.139.
Toloza-Villalobos J, Ignacio Arroyo J, Opazo J C. 2015. The circadian clock of teleost fish:a comparative analysis reveals distinct fates for duplicated genes. Journal of Molecular Evolution, 80(1):57-64, https://doi.org/10.1007/s00239-014-9660-x.
Urushibara N, Mitsuhashi S, Sasaki T, Kasai H, Yoshimizu M, Fujita H, Oda A. 2009. JNK and p38 MAPK are independently involved in tributyltin-mediated cell death in rainbow trout (Oncorhynchus mykiss) RTG-2 cells. Comparative Biochemistry and Physiology Part C:Toxicology & Pharmacology, 149(4):468-475, https://doi.org/10.1016/j.cbpc.2008.10.109.
Wang X, Han X, Zhang Y, Liu S S, Lin Q. 2019. Phylogenetic analysis and genetic structure of the seahorse, Hippocampus fuscus from the Arabian and Red Sea based on mitochondrial DNA sequences. Mitochondrial DNA Part A:DNA Mapping, Sequencing, and Analysis, 30(1):165-171, https://doi.org/10.1080/24701394.2018.1467410.
Wu X C, Chi X Q, Wang P M, Zheng D Q, Ding R, Li Y D. 2010. The evolutionary rate variation among genes of HOG-signaling pathway in yeast genomes. Biology Direct, 5:46, https://doi.org/10.1186/1745-6150-5-46.
Yang Z H. 2007. PAML 4:phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8):1586-1591, https://doi.org/10.1093/molbev/msm088.
Zhang Y H, Qin G, Zhang H X, Wang X, Lin Q. 2017. DNA barcoding reflects the diversity and variety of brooding traits of fish species in the family Syngnathidae along China's coast. Fisheries Research, 185:137-144, https://doi.org/10.1016/j.fishres.2016.09.015.
Zhu J, Cai L, Zhang T H, Chen L M, Jin P, Ma F. 2014. Identification and characterization of a p38-like gene from amphioxus (Branchiostoma belcheri):an insight into amphioxus innate immunity and evolution. Fish & Shellfish Immunology, 41(2):421-427, https://doi.org/10.1016/j.fsi.2014.09.028.
Copyright © Haiyang Xuebao